Bottom trawling in the deep sea is one of the main
drivers of sediment resuspension, eroding the seafloor and altering the
content and composition of sedimentary organic matter (OM). The physical and
biogeochemical impacts of bottom trawling were studied on the continental
slope of the Gulf of Castellammare, Sicily (southwestern Mediterranean),
through the analysis of two triplicate sediment cores collected at trawled
and untrawled sites (∼550 m water depth) during the summer of
2016. Geochemical and sedimentological parameters (excess 210Pb, excess
234Th, 137Cs, dry bulk density, and grain size), elemental
(organic carbon and nitrogen) and biochemical composition of sedimentary OM
(proteins, carbohydrates, lipids), as well as its freshness (phytopigments)
and degradation rates were determined in both coring locations. The
untrawled site had a sedimentation rate of 0.15 cm yr−1 and
presented a 6 cm thick surface mixed layer that contained siltier sediment
with low excess 210Pb concentrations, possibly resulting from the
resuspension, posterior advection, and eventual deposition of coarser and
older sediment from adjacent trawling grounds. In contrast, the trawled site
was eroded and presented compacted century-old sediment highly depleted in
OM components, which were between 20 % and 60 % lower than those in the
untrawled site. However, the upper 2 cm of the trawled site consisted of
recently accumulated sediments enriched in excess 234Th, excess
210Pb, and phytopigments, while OM contents were similar to those from
the untrawled core. This fresh sediment supported protein turnover rates of
0.025 d−1, which doubled those quantified in surface sediments of the
untrawled site. The enhancement of remineralization rates in surface
sediment of the trawled site was associated with the arrival of fresh
particles on a chronically trawled deep-sea region that is generally
deprived of OM. We conclude that the detrimental effects of bottom trawling
can be temporarily and partially abated by the arrival of fresh and
nutritionally rich OM, which stimulate the response of benthic communities.
However, these ephemeral deposits are likely to be swiftly eroded due to the
high trawling frequency over fishing grounds, highlighting the importance of
establishing science-based management strategies to mitigate the impacts of
bottom trawling.

Most of these impacts have been documented in shallow environments, where
sediment and OM fluxes are generally high and sediment resuspension and OM
remineralization induced by bottom trawling can be comparable to those
induced by natural high-energy events such as storms (Buscail et al., 1990;
Dellapenna et al., 2006; Ferré et al., 2008; Pusceddu et al., 2005b).
Since these natural physical disturbances are persistent, shallow benthic
communities generally present higher resilience to the impacts of bottom
trawling than communities that live in less disturbed areas, such as the
deep sea (Kaiser, 1998).

Contrary to the observed increases in total organic carbon on muddy
continental shelf trawling grounds (Palanques et al., 2014; Polymenakou et
al., 2005; Pusceddu et al., 2005a), the continuous removal of sediment by
trawlers on continental slopes has significantly impoverished bulk organic
carbon as well as its labile and fresh pools (Martín et al., 2014b;
Pusceddu et al., 2014; Sañé et al., 2013). The loss of organic
matter has also reduced organic carbon turnover rates on slope trawling
grounds, severely impacting the meiofauna and, at the same time, promoting
the abundance of taxa with opportunistic life strategies (Pusceddu et al.,
2014). However, the combined effect of bottom trawling erosion along with
the alteration of sedimentary organic matter, which usually represents the
fundamental energy source for commercial deep-sea benthic species, is not
fully understood.

The Gulf of Castellammare holds one of the most important bottom trawling
grounds in the northern Sicilian shore (southwestern Mediterranean Sea).
Bottom trawlers in this gulf operate using otter trawl gear, a trawling
technique which consists of dragging a wide net that is held open and in
contact with the seafloor by two otter doors (Martín et al., 2014a).
The first data of bottom trawlers in the area go back to the 1960s, but this
fishing technique has became more active since the 1980s (European Commission Fisheries
& Maritime Affairs, 2014), as a result of the modernization of the
Sicilian trawling fleet (L.R. 1/1980, 1980; L.R. 26/1987, 1987). Fishing stocks within
this gulf were declining alarmingly until the Sicilian government
established a trawling ban area in the inner shelf in 1990 (L.R. 25/1990, 1990),
delimited by the junction between Capo Rama and Torre dell'Uzzo (Fig. 1).
Since the establishment of this closure, both demersal biomass and catch per
unit effort (CPUE) of artisanal fisheries (non-towed bottom gear and pelagic
gear) have increased in that area (Pipitone et al., 2000; Whitmarsh et al.,
2002). However, bottom trawlers have been concentrating their efforts beyond
the restricted area in the mid-continental slope (>500 m depth),
leading to a decrease in CPUE since the trawl ban as a result of the
continuous overexploitation of fishing stocks (Arculeo et al., 2014;
Whitmarsh, 2002). A more recent management strategy aimed to prevent the
collapse of Sicilian fisheries established a 30 d bottom trawling closure
per year, which can occur from 1 August to 31 October (Decreto 1339/2001, 2001).

Figure 1Bathymetric map of the Gulf of Castellammare. Location of the
sediment cores sampled at the trawled (red circles) and untrawled (blue
squares) sites. Unfilled sampling points indicate unsuccessful sediment core
deployments. Seafloor images obtained from ROV dives are shown with
triangles (see Fig. S1). The distribution of trawling grounds as trawling
frequency (number of total hauls per grid area) in 2016 (1 January to
10 August) was calculated for a 200 m × 200 m grid. The limit of the
trawl banned area between Torre dell'Uzzo and Cape Rama is indicated by a
dashed line. The main trawling harbors (Castellammare del Golfo and Terrasini)
and the most relevant ephemeral rivers (San Bartolomeo, Nocella, and Jato)
are also annotated. The yellow arrow illustrates the direction of the
regional surface current.

Despite the numerous studies that address the effects of the trawl ban in
the Gulf of Castellammare (Fanelli et al., 2008; Romano et al., 2016;
Pipitone et al., 2000; Whitmarsh et al., 2002), no studies have yet assessed
the impacts of bottom trawling on the gulf's sedimentary environment. This
study aims to reveal whether erosion prevails in bottom trawling grounds and
what the consequent alterations on sedimentary organic matter are, by
comparing sediment cores collected at a trawled and untrawled site in the
Gulf of Castellammare. The degree of erosion will be estimated based on
sedimentological parameters and radioactive tracers with different
half-lives (210Pb, t1/2=22.3 years; 234Th, t1/2=24.1 d), whereas the alterations on sedimentary organic matter will be
determined based on its quantity, composition, and nutritional quality. The
coupled analyses of radioactive tracers and biomarkers will also provide
insights into the effects of the arrival of fresh sediment on impacted
trawling grounds.

2.1 Study area

The Gulf of Castellammare is one of the widest bays of the northern coast of
Sicily, with over 70 km of coastline, enclosed by Cape Rama to the east and
Cape San Vito to the west (Fig. 1). A cyclonic along-slope current dominates
the gulf's circulation at an average speed of 0.1–0.2 m s−1
on the upper continental shelf, which can sometimes reach maximum speeds of
0.4 m s−1 (Sarà et al., 2006). The seafloor morphology
consists of a subhorizontal gently sloping continental shelf that extends
approximately 5 km offshore. The continental slope is around
11∘ steep down to 500 m water depth, and it then gradually
decreases to around 1.5∘ at 1300 m water depth (Lo Iacono et
al., 2014). Several small, narrow submarine canyons cut the slope, breaching
the shelf break at 120 to 140 m depth (Lo Iacono et al., 2014). Small
seasonal torrents discharge into the gulf, namely the Nocella, Jato, and San
Bartolomeo rivers, with annual average discharges between 0.24 and 0.32 m3 s−1 (Regione
Siciliana, 2007). Storm-induced flash floods can cause short flushing events
of up to 1.2 m3 s−1 that transport significant amounts
of nutrients into the sea (Calvo and Genchi, 1989).

2.2 Sediment core sampling

In the framework of the FP7 EU-Eurofleets 2 ISLAND (ExplorIng SiciLian
CAnyoN Dynamics) cruise on board the R/V Angeles Alvariño, sediment cores were collected in
August 2016 from trawled and untrawled sites in the Gulf of Castellammare.
Sampling locations were selected based on the distribution of operating
trawlers using data from a vessel monitoring system (VMS) (see Sect. 2.8).
Sampling took place prior to the temporal fishing closure in the Gulf of
Castellammare, which took place that year between 17 September
and 16 October. This ensured that sediment cores reflect the
alterations caused by bottom trawling persisting in this deep environment.

A total of five multicore deployments were conducted using a K/C Denmark A/X
six-tube multicorer (inner diameter 9.4 cm) at trawled and untrawled sites
along the 550 m contour line. However, only one trawled and one untrawled
site could be sampled (Fig. 1), possibly due to high sediment compaction at
the trawled sites, as experienced by Martín et al. (2014b), and/or due to
the swell during the coring operation that could hamper a successful
triggering of the multicorer.

Triplicate sediment cores were retrieved at each site from three independent
multicore deployments to account for spatial variability of organic matter
analyses. The sediment cores were sliced on deck (0–1, 1–3, 3–5, 5–7, and
7–9 cm) and stored in calcinated aluminum foil at −20∘C until
analysis of organic matter content. At each site, a single sediment core
from one of the three deployments was reserved for sedimentary,
radiochemical, and elemental analyses. This sediment core was sliced on deck
at 1 cm intervals and kept in sealed plastic bags at −20∘C until being
freeze-dried in the laboratory for analyses.

Prior to sediment recovery, the remotely operated vehicle (ROV) Seaeye
Falcon, from the University of Plymouth (UK), collected visual evidence of
trawling impact at the trawled sampling site and of no impact at the control
site to corroborate the sampling strategy (Fig. S1 in the Supplement).

2.3 Sedimentary characteristics

Dry bulk densities of sediment cores were calculated by dividing the net dry
weight corrected for salt content by the sample volume. Grain size fractions
of sand (>63µm), silt (4–63 µm), and clay (<4µm) were obtained using a Horiba Partica LA-950V2 particle-size
analyzer, with an accuracy of 0.6 % and a precision of 0.1 %. Prior to
analysis, 1–4 g of sample was oxidized using 20 % H2O2 and
sediment particles were disaggregated with P2O7-.

2.4 Radiochemical analyses

Concentrations of 210Pb were determined through the analysis of its
decay product 210Po by alpha spectrometry following the method
described by Sanchez-Cabeza et al. (1998), assuming secular equilibrium of
both radionuclides at the time of analysis. Between 150 and 300 mg of
homogenized ground sample was spiked with 209Po as a chemical yield
and microwave-digested using concentrated HNO3, HF, and HBO3. The
resulting solutions were evaporated and reconditioned with 1 M HCl. Polonium
isotopes were spontaneously deposited onto silver disks while stirring at
70 ∘C for at least 8 h. Alpha emissions of 209Po (4883 keV) and 210Po (5304 keV) were quantified using passivated implanted
planar silicon (PIPS) detectors (CANBERRA, model PD-450.18 A.M.) and the
Genie™ data acquisition software. Supported concentrations of
210Pb in the sediment cores were obtained by averaging constant
concentrations of total 210Pb from the bottom of the core, from 2 to 37 cm for the trawled core and from 27 to 49 cm for the untrawled core,
assuming complete decay of excess 210Pb at these depths. Supported
210Pb concentrations were corroborated by measuring 226Ra
concentrations through its decay product 214Pb (295 and 352 keV) in
several samples along each core using gamma spectroscopy, using calibrated
geometries in a well-type high-purity germanium detector (CANBERRA, model
GCW3523).

Concentrations of 234Th were also measured with gamma spectroscopy
through the 63 keV emission line. Given its short half-life (24.1 d),
samples were measured within two half-lives (∼6 weeks) since
sampling, which only allowed the measurement of the upper 5 cm of the
trawled and untrawled cores. Samples were remeasured at least 6 months
later, after excess 234Th had decayed, to obtain supported 234Th
concentrations, equivalent to 238U concentrations. Excess 234Th
was calculated by subtracting supported 234Th from total 234Th,
accounting for 234Th decay and in-growth from 238U since sampling.

Concentrations of 137Cs were also quantified using gamma spectroscopy
through the emission line at 662 keV. Gamma measurements of the untrawled
sediment core were extended in depth to 20 cm, whereas in the trawled core
measurements were limited to the upper 5 cm since no 137Cs was detected
in that core.

2.5 Elemental analyses

Analyses of total carbon, organic carbon (OC), and total nitrogen (TN) were
carried out with an elemental analyzer (Costech ECS analyzer 4010),
according to the procedure described in Nieuwenhuize et al. (1994). Samples
for OC analysis were first decarbonated by acid-fuming the samples in the
presence of 12 N HCl for 24 h and repeatedly adding 100 µL of 2 N HCl to the sample until effervescence ceased. Inorganic carbon (IC),
quantified as the difference between total carbon and organic carbon, was
converted to calcium carbonate (CaCO3) concentrations using the
molecular mass ratio of CaCO3:IC (100 ∕ 12), assuming all inorganic
carbon present is in the form of CaCO3. To account for analytical
error, replicate analyses were performed for samples every 5 cm throughout
the cores. An average percentage error of 1.2 % was obtained for carbon
whereas nitrogen presented a slightly higher average percentage error of 1.9 %.

2.6 Biochemical composition of sedimentary organic matter

Total proteins, carbohydrates, and lipids were quantified
spectrophotometrically (Varian Cary® 50 UV-Vis) according to
the methods described in Hartree (1972) and modified by Rice (1982),
Gerchakov and Hatcher (1972), Bligh and Dryer (1959), and Marsh and
Weinstein (1966). The analyses of proteins and lipids were carried out on
0.1–0.6 g of frozen sediment, whereas carbohydrate analyses were performed on
previously dried sediment. Protein, carbohydrate and lipid contents were
transformed into carbon equivalents using 0.49, 0.4, and 0.75 mgC mg−1 as conversion factors, respectively, and their sum reported as
biopolymeric C (Fabiano et al., 1995). Chlorophyll a and phaeopigments,
after extraction with 90 % acetone, were quantified fluorometrically
(Shimadzu RF-6000) according to Lorenzen and Jeffrey (1980) and modified by
Danovaro (2010) for sediments. Total phytopigment concentrations were
defined as the sum of chlorophyll a and phaeopigment concentrations and
converted into carbon equivalents using a conversion factor of 40 (Pusceddu
et al., 2010).

2.7 Sedimentary OM freshness and degradation rates

The contribution of phytopigment to biopolymeric C was used as a proxy to
estimate OM freshness: since in the deep sea there is no in situ primary
production, higher values of this ratio are associated with
recently deposited material of algal origin (Pusceddu et al., 2010).

Since N is the most limiting factor for heterotrophic nutrition and proteins
are N-rich products, sedimentary OM degradation was estimated using the
degradation rate of proteins, obtained from the analysis of extracellular
aminopeptidase activities. Aminopeptidase activity was estimated
fluorometrically after incubation of approximately 0.1 g of sediment with
100 µM L-leucine-4-methylcumarinyl-7-amide for 1 h in the dark. This
substrate, when exposed to extracellular aminopeptidase, produces
fluorescence with an intensity proportional to the enzyme activity.
Fluorometric analyses were carried out before and after incubation, and the
difference was used to calculate protease activities (Danovaro, 2010). The
results were converted to carbon equivalents using the conversion factor of
72 ngC nmol protease−1 (Fabiano and Danovaro, 1998).
Turnover rates were then calculated by dividing protein-C degradation rates
by protein-C sedimentary contents.

2.8 Trawling effort from VMS data

Fishing intensity of the Italian bottom trawling fleet was obtained using
data provided by the vessel monitoring system (VMS), the main tracking device
used for monitoring fishing activities. According to the Common Fisheries
Policy of the European Union (European Commission, 2003), fishing vessels
with overall length equal to or larger than 15 m must be equipped with a
VMS transmitter, called “Blue Box”. It estimates the position of the
vessel using the Global Positioning System and sends this information, along with
the speed and heading of the vessel, to the network of the coastal guard by
Inmarsat C to the Fishing Monitoring Centre in less than 10 min at 2 h
time intervals. Fishing intensity was calculated using yearly VMS data from
2007 to 2015, whereas for 2016, only VMS data from 1 January to
10 August were taken into account, prior to sampling. Trawling
frequency was represented as the number of times trawled per grid cell (200 m × 200 m) during each year. The native VMS data were processed using the R package VMSbase (Russo et al., 2014). The size of the grid was defined
considering the error associated with the reconstruction of the trawling hauls
as described by Russo et al. (2011).

2.9 Statistical analyses

Statistical analyses were used to test whether OM quantity and biochemical
composition (protein, carbohydrate, lipid, and phytopigment concentrations),
freshness (the phytopigment-to-biopolymeric C ratio), and degradation rates
(sedimentary protein turnover rates) were statistically different between
trawled and untrawled sites in the upper 9 cm of sediment cores. The
analysis consisted of two orthogonal factors: site (trawled vs. untrawled)
and depth in the sediment (five levels: 0–1, 1–3, 3–5, 5–7, 7–9 cm). Permutational analyses of variance (PERMANOVA), in either the
univariate (variable by variable) or multivariate contexts, were based on
Euclidean distances of previously normalized data using 999 permutations of
residuals with unrestricted permutation of raw data (univariate tests) or
under a reduced model (multivariate tests) (Anderson, 2001). Since for almost
all tests the interaction between factors was significant, we conducted
post hoc permutational pairwise comparison tests between trawled and
untrawled sites for each sediment layer and among sediment layers for
trawled and untrawled sites, separately. Given the restricted number of
unique permutations, p values were obtained from Monte Carlo simulations
(Anderson and Robinson, 2003). Bi-plots produced after canonical analysis of
principal components (CAP) were used to visualize the differences between
trawled and untrawled samples in terms of organic matter biochemical
composition (Anderson and Willis, 2003). All statistical analyses were
performed using the routines included in the PRIMER 6+ software.

Table 1Summary of the main parameters of the trawled and untrawled cores. Data
for grain size, CaCO3, OC, TN, and OC∕TN correspond to average values
±1 standard deviation of that layer. MAR: mass accumulation rate;
SAR: sediment accumulation rate.

Bottom trawling in the Gulf of Castellammare is limited to the mid-slope
(>500 m), beyond the trawling-ban area. In the main bottom
trawling ground, where the trawled core was retrieved, hauls generally
follow the contour lines in a W–E direction (Fig. 1). Fishing effort has
generally increased since 2007, with a predominating trawling frequency of 1
to 40 hauls per grid cell during that year, which then increased to around
60 to 100 hauls per grid cell since 2013 (Fig. S2). A smaller trawling
ground has opened since 2012 towards the eastern side of the gulf, close to Cape
Rama (Figs. 1, S2). Although trawling frequency for 2016 was only computed
from January to August, this year presented the highest fishing effort in
comparison to the previous years.

3.1 Physical characteristics

The untrawled sediment core presented an excess 210Pb concentration
profile that extended to 25 cm in depth, with a total inventory of 17 900 ± 900 Bq m−2 (Fig. 2a; Table 1). In the upper 6 cm,
excess 210Pb concentrations slightly decreased towards the surface from
372±22 Bq kg−1 to 272±15 Bq kg−1 (Fig. 2a). Below, excess 210Pb concentrations presented a
continuous decrease between 6 and 25 cm, from which an average sediment
accumulation rate of 0.090±0.003 g cm−2 yr−1, equivalent to 0.151±0.005 cm yr−1
(R2=0.995) (Table 1), was calculated applying the Constant Flux : Constant Sedimentation model (CF : CS; Krishnaswamy et al., 1971). This
sedimentation rate was independently validated by 137Cs. Detectable
concentrations of 137Cs appeared at 17 cm depth, which was ascribed to
the first detonations of thermonuclear weapons in the early 1950s. Above,
137Cs concentrations depicted a broad concentration maximum at 8–13 cm,
centered at 10–11 cm. This maximum was attributed to the combined
accumulation of the maximum fallout prior to the cessation of nuclear
atmospheric testing in 1963 as well as the deposition of 137Cs emitted
from the Chernobyl accident in 1986 (Fig. 2a). The deposition of 137Cs
from each of these events could not be distinguished due to the low
sedimentation rate and the sampling resolution of this core. Concentrations
of excess 234Th ranged between 71 and 97 Bq kg−1
between 2 and 5 cm, decreased to 37±7 Bq kg−1 at 1–2 cm and was not detected on surface sediments (0–1 cm) of the core (Fig. 2b).
The penetration depth of excess 234Th could be greater than the upper 5 cm analyzed, leading to an inventory of at least 1080 Bq m−2
(Table 1). Dry bulk density of the untrawled site remained constant in the
upper 7 cm at ∼0.5 g cm−3, gradually
increased to ∼0.7 g cm−3 at 15 cm, and then
remained relatively constant with depth (Fig. 2c). The upper 6 cm presented
coarser grain size consisting of higher silt (77 %) and lower clay (22 %) fractions, in comparison to the rest of the core, which had lower silt
(44 %) and higher clay (54 %) fractions (Fig. 2c, Table 1). CaCO3
concentrations were constant in the upper 10 cm, with an average
concentration of 18.4±0.4 %, decreased to ∼15 %
at 15–20 cm, and then slightly increased with depth until ∼20 % at 30 cm (Fig. 4d).

3.2 Sedimentary organic matter

Trawled and untrawled sediment cores presented different OC and TN
concentration profiles (Fig. 4). The untrawled core had OC concentrations of
∼0.9 % in the upper 20 cm, which then decreased to
∼0.8 % at 35 cm. In contrast, the trawled core presented
OC concentrations that fluctuated between ∼0.8 % and
∼0.7 % with depth. Similarly, concentrations of TN in the
untrawled core were ∼0.13 % in the upper 20 cm, which then
decreased to ∼0.10 % at 35 cm, whereas the trawled core
presented TN concentrations varying between ∼0.11 % and
∼0.09 % with depth. For both OC and TN, concentrations in
the upper 20 cm were ∼20 % lower at the trawled site in
comparison to the untrawled site, reaching similar concentrations at 30 cm
in depth (Fig. 4). Profiles of the OC∕TN ratio presented similar values at both
sites, varying between 6.5 and 7.5 throughout the core (Fig. 4c).

In general, organic matter quantity was higher at the untrawled site than at
the trawled site, with the exception of surface layers, which presented
similar concentrations at both sites (Fig. 5). Protein concentrations at the
untrawled site were 1.5 mgC g−1 in the upper 3 cm,
increased to maximum concentrations of ∼3 mgC g−1 at 3–7 cm, and decreased to 2.4 mgC g−1 at 7–9 cm.
The trawled site had similar ∼1.5 mgC g−1
protein concentrations in surface sediment that increased to almost 2.5 mgC g−1 in the deepest layer analyzed (Fig. 5a). Carbohydrate
concentrations at the untrawled site presented decreasing concentrations
from between 0.7 and 0.9 mgC g−1 in the upper 3 cm to 0.44 mgC g−1 in the deepest layer, whereas the trawled site had
constant concentrations of 0.42 mgC g−1 in the upper 9 cm
of the trawled site (Fig. 5b). Untrawled and trawled sites had similar lipid
concentrations of ∼0.6 mgC g−1 in the
topmost sediment layer, decreasing to 0.34±0.03 and 0.17±0.01 mgC g−1 at 7–9 cm of the
untrawled and trawled cores, respectively (Fig. 5c). Biopolymeric C
concentrations were constant (2.5±0.1 mgC g−1) along
the upper 9 cm of the trawled core, whereas concentrations increased in the
untrawled core from 2.9±0.2 mgC g−1 in the topmost
layer to ∼4 mgC g−1 in the 3–7 cm layer,
before returning to similar values observed in the surface layer (Fig. 5d).
At both sites, phytopigment profiles showed decreasing trends, with a
sharper decrease at the trawled site from 126±7µgC g−1 in the top layer to relatively constant values of 39±5µgC g−1 below 3 cm, whereas the untrawled
site showed a gradual decrease from 161±18µgC g−1 in
the topmost layer to 77±12µgC g−1 in the deepest one
(Fig. 5e).

Statistical analyses of the data indicated that both sampling site and core
depth had significant effects on the quantity of sedimentary OM (Table S1).
The post hoc comparison tests (Table S2) demonstrated that OM contents
between trawled and untrawled sites were generally statistically different
only below the topmost sediment layer (0–1 cm), with the exception of
carbohydrates.

Variations in the biochemical composition of sedimentary OM in terms of
protein, carbohydrate, lipid, and phytopigment contents were assessed
through PERMANOVA testing (Table S3). The results revealed that the biochemical
composition of sedimentary OM not only differed between trawled and
untrawled sites, but that these differences varied depending on the depth in
the core. The consequent post hoc pairwise tests between the trawled and
untrawled sites at all sediment layers indicated that the biochemical
composition of sedimentary OM, similar to the OM content, varied
significantly between trawled and untrawled sites at all depths, excluding
surface sediments (Table S4). The bi-plot produced after the canonical
analysis of principal components (Fig. 6) revealed that the vertical
variations in the biochemical composition of sedimentary OM in the untrawled
sediment core are greater than those observed at the trawled site, as
observed from the greater spatial distribution of these samples. However,
the proximity of superficial samples of trawled cores to most of the
untrawled samples in the bi-plot illustrates a resemblance in their
biochemical composition.

Figure 6Variations in the biochemical composition of the sedimentary
organic matter. Bi-plot after canonical analysis of the principal
coordinates. Note that symbols represent the same core depth for both
trawled (red) and untrawled (blue) sites and that increasing depth is also
illustrated by a fading filling.

The contributions of phytopigment to biopolymeric C and the protein turnover
rates at trawled and untrawled sites are given in Table S5 and illustrated
in Fig. 7. The relative contribution of phytopigments to biopolymeric C was
similar in superficial sediments of trawled and untrawled sites, with
relatively high values (∼5 %) that decreased with depth at
both sites, although more pronouncedly at the trawled site, reaching
∼1.4 % at 5–7 cm, than at the untrawled site, reaching 2.5 % at 7–9 cm (Fig. 7a). Turnover rates were significantly higher in the
upper 3 cm of the trawled site (0.017–0.025 d−1) in comparison to
∼0.015 d−1 of the superficial sediment of the untrawled
site (Table S5b, Fig. 7b). Below, turnover rates decreased to
∼0.005 d−1 for both sites.

4.1 Long-term impacts of intense bottom trawling

Evidence of the long-term impacts of intense bottom trawling are clear at a
trawled site of the Gulf of Castellammare. ROV images from the trawled area
present a barren seafloor, with several deep linear furrows hundreds of
meters long and up to 70 cm deep, presumably caused by the trawling gear's
heavy otter doors (Fig. S1a). The shallow penetration depth of excess
210Pb in the trawled core suggests that only the upper 2 cm of sediment
had been recently deposited on top of highly compacted sediments (0.7–0.8 g cm−3) that had accumulated more than 100 years ago,
considering the absence of excess 210Pb (Fig. 3a, c). These
sedimentological patterns are characteristic of a seafloor eroded by
trawling activities, as observed in other trawled regions with shallow
horizons of excess 210Pb and exposed over-consolidated, century-old
sediments (Martín et al., 2014b; Oberle et al., 2016; Paradis et al.,
2017, 2018). The uprooting of old sediment at this trawled site, with only a
thin accumulation of recent sediment in superficial layers, reveals that the
rate of sediment erosion induced by the high trawling frequency is greater
than sediment accumulation rates in the Gulf of Castellammare. Furthermore,
the coincident penetration depth of both excess 210Pb and excess
234Th at the trawled site (Fig. 3a, b) indicates that the accumulation
of fresh sediment would have occurred after the passage of the last trawler
over the sampling area and thus reveals that trawling frequency controls
the residence time of fresh sediment in these trawling grounds.

In contrast, excess 210Pb inventories were 2 orders of magnitude
higher in the untrawled core. This core had a sedimentation rate of 0.151±0.005 cm yr−1, comparable to those quantified at
similar depths in the Mediterranean Sea (DeGeest et al., 2008; Miralles et
al., 2005; Sanchez-Cabeza et al., 1999). The upper 6 cm of this core had
excess 210Pb concentrations that slightly decreased towards the
surface, a deep penetration depth of excess 234Th, and low dry bulk
densities (Fig. 2a, b), altogether signs of biological mixing (Arias-Ortiz,
et al., 2018; Pope et al., 1996; van Weering et al., 1998). The influence of
bioturbation at this site is corroborated by the presence of several burrows
directly observed during ROV dives prior to sampling (Fig. S1b). Sediment
mixing caused by bioturbation could explain the broad137Cs
concentration maximum observed at 8–13 cm, attributed to the combined
accumulation of 137Cs from the 1986 Chernobyl accident and from the
1963 global fallout, as well as diluting the 1954 signal with depth (Fig. 2a). However, bioturbation alone cannot account for the coarsening of
sediment observed in the upper 6 cm (Fig. 2c; Table 1). Provided the high
capacity of bottom trawling gear to resuspend sediments (Martin et al.,
2014a, c; Oberle et al., 2018; Puig et al., 2012), the siltation of
superficial sediments on the untrawled site could be explained by the
preferential deposition of siltier particles resuspended from an adjacent
trawling ground located ∼1 km up-current from this sampled
site (Fig. 1). Finer clay particles resuspended by bottom trawlers can be
advected to farther distances along the margin (Linders et al., 2017). This
siltier sediment would have been posteriorly redistributed and preserved
within the surface mixed layer of the untrawled site (Fig. 1).

Excluding the fresh superficial layers of the trawled site, the chronic
erosion induced by bottom trawling resuspension considerably depleted the
trawled site of both OC and TN by ∼20 % in comparison to
the untrawled site (Fig. 4; Table 1). Concentrations of OC and TN were
similar in the deeper layers of both sites, where sediments would have
accumulated more than a century ago, revealing that bottom trawling
re-exposes old sediment impoverished in OM (Fig. 4; Table 1). Similarly, the
trawled site had lower proteins (−5 % to −38 %), carbohydrates (−13 % to −58 %), lipids (−36 % to −52 %), biopolymeric carbon (−12 % to −37 %), and
phytopigments (−53 % to −67 %) than the untrawled site, with the exception
of superficial layers (Fig. 5). These results are in accordance with
previous studies that showed comparable losses of organic matter in slope
trawling grounds, reinforcing the concept that chronic and intensive bottom
trawling depletes these deep-sea sedimentary habitats of organic matter,
promoting their degradation over time (Martín et al., 2014b; Pusceddu et
al., 2014; Sañé et al., 2013).

4.2 Effects of the arrival of fresh sediment

During the ISLAND cruise, ROV dives showed high settling fluxes of large
particulate matter aggregates to the seafloor (Fig. S1). At both sampled
sites, evidence of recent accumulation of surface sediments was provided by
the presence of excess 234Th and high concentrations of phytopigments
(Fig. 5e), a compound that usually represents the most important food source
for deep-sea heterotrophic consumption (Pusceddu et al., 2010; Stephens et
al., 1997). This indicates that the Gulf of Castellammare was receiving
highly nutritious organic matter inputs during the sampling period. Indeed,
both the composition of sedimentary organic matter and the relative
contribution of phytopigment to biopolymeric C were similar in the fresh
superficial sediments at both trawled and untrawled sites. However, the
subsurface, century-old sediments of the trawled site have distinctively
different organic matter composition and significantly lower nutritional
quality in comparison to its untrawled counterpart (Figs. 6, 7a). This
suggests that, aside from the ephemeral deposition of fresh OM that will be
swiftly eroded by bottom trawlers' gear, deep-sea trawling grounds are
generally characterized by nutritionally poor organic matter contents
(Pusceddu et al., 2014; Sañé et al., 2013), which increases the
dependence on the supply of fresh OM in order to sustain benthic
communities. This hypothesis is corroborated by the higher OM turnover rates
in surface sediment of the trawled site in comparison to the untrawled site
(Fig. 7b), which reveal a prompt stimulation of microbial activities
resulting from the recent accumulation of fresh and nutritionally enriched
OM on the trawled site. In fact, benthic communities in areas that have
severe nutrient limitations, such as in eroded sediment of this trawled site
or in oligotrophic deep-sea regions, react instantaneously to food pulses
(Bett et al., 2001; Fabiano et al., 2001; Witte et al., 2003). In contrast,
the untrawled site is characterized by relatively higher total organic matter
contents as well as fresh and bioavailable compounds throughout the core,
possibly due to a deeper penetration of labile material through biological
mixing (Fig. 5). However, these sections also presented slowly decreasing
concentrations of phytopigment to biopolymeric C with depth as well as lower
protein turnover rates, revealing that this unstressed environment has a
lower consumption of labile OM and a relatively reduced dependence on the
arrival of fresh OM (Fig. 7a).

The higher OM turnover rates observed in the freshly deposited surface
layers of the trawled site also indicate a greater efficiency of OM
consumption and remineralization in the trawling ground in comparison to the
untrawled site. This enhanced mineralization through self-priming can occur
when fresh and degradable organic matter, such as fresh phytoplankton,
arrives to areas with more refractory compounds (Canfield, 1994; van
Nugteren et al., 2009), as was observed in a shallow trawling-disturbed area
in the southern North Sea, off the Belgian coast (van de Velde et al.,
2018). Similarly, bottom trawling in the shallow Thermaikos Gulf (Aegean
Sea) intensified microbial activities, which enhanced nutrient cycling and
organic carbon mineralization (Polymenakou et al., 2005; Pusceddu et al.,
2005a). This could have been attributed to the combined effect of
trawling-induced mixing of superficial labile OM with more degraded
subsurface OM, along with the continuous arrival of fresh OM to these
shallow continental shelves (Buscail et al., 1990; Tselepides et al., 2000).

In contrast, surface sediments collected in a deeper and intensely trawled
flank of La Fonera Canyon, in the NW Mediterranean margin, presented
significantly lower turnover rates than the nearby untrawled grounds
(Pusceddu et al., 2014). However, those sediment cores did not present signs
of recently accumulated sediment as observed at our sampling sites, further
proving the dependence on the arrival of fresh and nutritionally rich
sediment in intensely trawled grounds to support benthic organisms living in
these impacted deep-sea environments.

The high nutritional quality and OM turnover rates in recently accumulated
sediments from the trawled site suggest that high OM fluxes could help deep
bottom trawling grounds recover the nutritional characteristics of
sedimentary OM. These results confirm that actions aimed at mitigating the
impacts of bottom trawling include the implementation of temporary fishing
closures, allowing for a longer-lived deposition of fresh OM on the
seafloor. However, such temporary trawling closures would most probably not
allow the full restoration of fresh sediment from trawl-induced erosion,
given the low sedimentation rates found in these deep environments. Further
management strategies would need to be implemented to mitigate the impacts
of bottom trawling erosion (Depestele et al., 2018), which would magnify the
effect of temporary closures on the restoration of sedimentary OM in
nutrient-deprived trawling grounds.

Chronic and intense deep bottom trawling in the Gulf of Castellammare erodes
large volumes of sediment, exposing century-old, compacted sediment
that is depleted in OM. This continuous erosion limits the accumulation of
fresh sediment since any recently deposited particulate matter is promptly
removed due to the high trawling frequency. Nevertheless, we present
evidence that the short-lived deposition of recent and nutritionally rich
organic matter leads to high turnover rates of labile OM. Our results
emphasize that nutrient-deprived and eroded deep bottom trawling grounds are
highly dependent on the arrival of fresh and nourishing particulate organic
matter to sustain benthic communities, which can temporarily and partially
abate the detrimental effects of bottom trawling in superficial sediment.

SP, AP, PP, and CLI designed the scientific study. SP and CLI retrieved the
samples. SP and DM performed the analyses and TR processed the fishing
effort data. SP wrote the paper. All authors contributed to the
interpretation and discussion of the results, as well as the revision of the
paper.

The results presented in this study were obtained within the Exploring
SiciLian CAnyoN Dynamics (ISLAND) project and the Assessment of Bottom-trawling Impacts in DEep-sea Sediments (ABIDES) Spanish Research Project.
We would like to thank the crew of the R/V Ángeles Alvariño and the
ISLAND cruise team that helped collect the samples. This work is
contributing to the Institut de Ciència i Tencologia Ambientals “Unit of
Excellence”. Sarah Paradis is supported by a predoctoral FPU
grant from the Spanish government.

This research has been supported by the European Commission, Seventh Framework Programme (EUROFLEETS2 (grant no. 312762)), the Ministerio de Economía y Competitividad (grant no. CTM2015-65142-R), the Generalitat de Catalunya (2017 SGR-863 and 1588), the Australian Research Council (LIEF project (grant no. LE170100219)), the Ministerio de Economía y Competitividad (grant no. MDM2015-0552), and the Ministerio de Educación, Cultura y Deporte (grant no. FPU14/07039).

Chronic deep bottom trawling in the Gulf of Castellammare (SW Mediterranean) erodes large volumes of sediment, exposing over-century-old sediment depleted in organic matter. Nevertheless, the arrival of fresh and nutritious sediment recovers superficial organic matter in trawling grounds and leads to high turnover rates, partially and temporarily mitigating the impacts of bottom trawling. However, this deposition is ephemeral and it will be swiftly eroded by the passage of the next trawler.